Detection of FOX-AmpC-β-lactamase gene and antibiogram of AmpC-beta-lactamase-producing pathogens isolated from chronic suppurative otitis media patients in Nigeria
-
Ibiam Francis Amadi
,
Obasikene Catherine Nchedo
,
Ariom Thaddaeus Obaji
,
Monday Agbonifo
,
Egwu Eze
,
Iroha Chidinma Stacy
,
Moses Ikechukwu Benjamin
,
Iroha Ifeanyichukwu Romanus
Abstract
Background and Objectives: AmpC-producing Gram-negative bacterial (GNB) pathogens are distributed worldwide, especially in clinical settings. This study aimed to determine the antibiogram and the type of AmpC-β-lactamase gene harboured by GNB pathogens implicated in chronic suppurative otitis media (CSOM) cases.
Materials and Methods: Ear swab samples (300) collected from patients with active CSOM were analysed using standard microbiological techniques. Phenotypic and molecular detection of AmpC β-lactamase production was done by cefoxitin/cloxacillin double-disk synergy test and PCR respectively. Antibiogram was determined by disk diffusion technique.
Results: Among the GNB pathogens isolated from CSOM patients, P. aeruginosa was the most predominant (36.3%); followed by K. pneumoniae (22.3%), and E. coli (13.7%). Patients with active CSOM showed increased bacteria isolation rate from bilateral ear discharges than unilateral ear discharges. E. coli and P. aeruginosa were more prevalent among patients with duration of discharge >2 weeks; recording 9.0% and 20.3% respectively. AmpC β-lactamase producers accounted for 14.0%; they were highly resistant (60%-100%) to cephalosporins, trimethoprim-sulfamethoxazole, ofloxacin, amoxicillin, and tetracycline, but very susceptible (70.4%-100%) to ciprofloxacin, imipenem, and amikacin. Multiple antibiotic resistance indices of isolates ranged from 0.7-0.8. FOX-AmpC-β-lactamase gene was detected in 3.9% of the isolates.
Conclusion: The detection of AmpC β-lactamase-producing multidrug-resistant GNB pathogens harbouring FOX-AmpC-β-lactamase gene among patients with CSOM infections in our study is a serious public health problem which needs urgent intervention.
1. Kashyap S, Pandey A, Thakuria B, Saxena AK, Asthana AK, Madan M. Resistant microorganisms isolated from cases of chronic suppurative otitis media: A therapeutic concern. Nat J Lab Med 2017; 6: MC01-MC06.
2. Endaylalu K, Abera B, Mulu W. Extended spectrum beta lactamase producing bacteria among outpatients with Ear infection at FelegeHiwot Referral Hospital, North West Ethiopia. PLoS One 2020; 15 (9): e0238891.
3. Buhaibeh Q, Dhaiban T, Alyafei E, Al-Jundi Abdulsalam AS. Bacterial profile and antimicrobial susceptibility patterns of otitis media among children in Qatar. Int J Res Med Sci 2019; 7: 3311-3316.
4. Ejiofor SO, Edeh AD, Ezeudu CE, Gugu TH, Oli AN. Multi-drug resistant acute otitis media amongst children attending out-patient clinic in Chukwuemeka Odumegwu Ojukwu University Teaching Hospital, Awka, South-East Nigeria. Adv Microbiol 2016; 6: 495-501.
5. Tesfa T, Mitiku H, Sisay M, Weldegebreal F, Ataro Z, Motbaynor B, et al. Bacterial otitis media in sub-Saharan Africa: A systematic review and meta-analysis. BMC Infect Dis 2020; 20: 225.
6. Akinjogunla OJ, Eghafona NO, Enabulele IO. Aetiologic agents of acute otitis media (AOM): prevalence, antibiotic susceptibility, beta-lactamase (Βl) and extended spectrum beta-lactamase (ESBL) production. J Microbiol Biotechnol Food Sci 2011; 1: 333-353.
7. Khatoon A, Rizvi M, Sultan A, Khan F, Sharma M, Shukla I, et al. Chronic suppurative otitis media: A clinico-microbiological Menace. Int J Res Med Sci 2015; 3: 1932-1936.
8. Teklu DS, Negeri AA, Legese MH, Bedada TL, Woldemariam HK, Tullu KD. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrob Resist Infect Control 2019; 8: 39.
9. Pfeifer Y, Cullik A, Witte W. Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 2010; 300: 371-379.
10. Walsh TR, Toleman MA, Poirel L, Nordmann P. Metallo-β- lactamases: The Quiet before the storm? Clin Microbiol Rev 2005; 18: 306-325.
11. El-Hady SA, Adel LA. Occurrence and detection of AmpC β-lactamases among Enterobacteriaceae isolates from patients at Ain Shams University Hospital. Egypt J Med Hum Genet 2015; 16: 239-244.
12. Chika E, Charles E, Ifeanyichukwu I, Michael A. First Detection of FOX-1 AmpC β-lactamase gene expression among Escherichia coli isolated from abattoir samples in Abakaliki, Nigeria. Oman Med J 2018; 33: 243-249.
13. Nnaji JO, Moses IB, Ejikeugwu PC, Nwakaeze EA, Ude-Ude I, Iroha IR. Antibiogram and molecular characterization of AmpC and ESBL-producing Gram-negative bacteria from poultry and abattoir samples. Pak J Biol Sci 2021; 24: 193-198.
14. Orji JN (2011). Political Organization in Nigeria since the Late Stone Age: A History of the Igbo People, Palgrave Macmillan, 2011th Edition, New York.
15. The World Gazetteer (2013). https://archive.is/20130209150810/http://www.world-gazetteer.com/wg.php. Accessed 10 November, 2022.
16. Molla R, Tiruneh M, Abebe W, Moges F. Bacterial profile and antimicrobial susceptibility patterns in chronic suppurative otitis media at the University of Gondar Comprehensive Specialized Hospital, Northwest Ethiopia. BMC Res Notes 2019; 12: 414.
17. World Medical Association (WMA). Declaration of Helsinki. Ethical principles for medical research involving human subjects. Note of Clarification on paragraph 30 added by the WMA General Assembly, Tokyo; 2004.
18. Cheesbrough M (2006). District Laboratory Practice in Tropical Countries (Part II), Cambridge University.
19. Moses IB, Ugbo EN, Odah EE, Iroha IR, Agumah NB, Ukpai EG, et al. Antibiogram and phenotypic characterization of E. coli isolated from Nigeria’s paper currencies obtained from Butchers in Ebonyi State. Arch Clin Microbiol 2018; 9: 85.
20. Iroha IR, Mohammed ID, Moses IB, Ngwu NJ, Uzoeto HO, Oladimeji AS, et al. Molecular characterization of Enterobacteriaceae isolated from gingivitis and periodontitis patients and the antimicrobial activity of mouth wash agents. Sci Afr 2022; 15: e01106.
21. Clinical Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 27th Edition, CLSI supplements M100Wayne: Clinical and Laboratory Standards Institute; 2017.
22. Moses IB, Esimone CO, Iroha IR, Ugbo EN, Orji JO, Nwuzo AC, et al. First report on the antibiotic resistance profiles and virulence genes of Staphylococcus pseudintermedius colonizing dogs and humans in Abakaliki, South-East Nigeria. Res J Microbiol 2020; 15: 22-34.
23. Moses IB, Esimone CO, Iroha IR, Rubin JE, Sniatynsky MK, Ribeiro ACS, et al. Antibiotypes and high frequency of toxin genes in methicillin-resistant Staphylococcus pseudintermedius from nares of dogs and dog guardians in Nigeria. Comp Immunol Microbiol Infect Dis 2022; 89: 101870.
24. Singh BR, Pradhan S, Murthy R, Agrawal E, Barapatre R, Kumari N, et al. Emergence of antibiotic resistance in bacteria isolated from Tubotympanic type of chronic suppurative otitis media in Chhattisgarh. Int J Otorhinolaryngol Head Neck Surg 2019; 5: 1674-1678.
25. Fayemiwo SA, Ayoade RA, Adesiji YO, Taiwo SS. Pattern of bacterial pathogens of acute otitis media in a tertiary Hospital, South Western Nigeria. African J Clin Exp Microbiol 2017; 18: 29- 34.
26. Nnebe-Agumadu U, Okike O, Orji I, Ibekwe RC. Childhood suppurative otitis media in Abakaliki: isolated microbes and in vitro antibiotic sensitivity pattern. Niger J Clin Pract 2011; 14: 159-162.
27. Prakash R, Juyal D, Negi V, Pal S, Adekhandi S, Sharma M, et al. Microbiology of chronic suppurative otitis media in a tertiary care setup of Uttarakhand State India. N Am J Med Sci 2013; 5: 282-287.
28. Kazeem MJ, Aiyeleso R. Current Bacteriological Profile of chronic suppurative otitis media in a tertiary facility of Northern Nigeria. Indian J Otol 2016; 22: 157-161.
29. Chirwa M, Mulwafu V, Aswani JM, Masinde V, Mkakosya R, Soko D. Microbiology of chronic suppurative otitis media at Queen Elizabeth Central Hospital, Blantyre, Malawi: A cross-sectional descriptive study. Malawi Med J 2015; 27: 120-124.
30. Amiri-Andy SA, Sarokhani D, Azami M, Vazini H, Rezaei-Tavirani M, Dehkordi AH. Systematic review and meta-analysis of otitis media in Iran: prevalence, etiology, antibiotic susceptibility, and complications. Indian J Otol 2018; 24: 1-8.
31. Gupta P, Varshney S, Kumar SK, Mohanty A, Jha MK. Chronic suppurative otitis media: A microbiological review of 20 years. Indian J Otol 2020; 26: 59-67.
32. Mansoor T, Musani MA, Khalid G, Kamal M. Pseudomonas aeruginosa in chronic suppurative otitis media: sensitivity spectrum against various antibiotics in Karachi. J Ayub Med Coll Abbottabad 2009; 21: 120-123.
33. Poorey VK, Iyer A. Study of bacterial Flora in chronic suppurative otitis media and its clinical significance. Indian J Otolaryngol Head Neck Surg 2002; 54: 91-95.
34. Adesoji AT, Ogunjobi AA, Olatoye IO. Molecular characterization of selected multidrug resistant Pseudomonas from water distribution systems in southwestern Nigeria. Ann Clin Microbiol Antimicrob 2015; 14: 39.
35. Onuoha SC. The prevalence of antibiotic resistant diarrhogenic bacterial species in surface waters, South Eastern Nigeria. Ethiop J Health Sci 2017; 27: 319-330.
36. Onifade AK, Afolayan CO, Afolami OI. Antimicrobial sensitivity, extended spectrum beta-lactamase (ESBL) production and plasmid profile by microorganisms from otitis media patients in Owo and Akure, Ondo State, Nigeria. Karbala Int J Mod Sci 2018; 4: 332-340.
37. Manoharan A, Sugumar M, Kumar A, Jose H, Mathai D, Khilnani GC, et al. Phenotypic & molecular characterization of AmpC β-lactamases among Escherichia coli, Klebsiella spp. & Enterobacter spp. from five Indian Medical Centers. Indian J Med Res 2012; 135: 359-364.
38. Helmy MM, Wasfi R. Phenotypic and molecular characterization of plasmid mediated AmpC β-lactamases among Escherichia coli, Klebsiella species, and Proteus mirabilis isolated from urinary tract infections in Egyptian hospitals. Biomed Res Int 2014; 2014: 171548.
2. Endaylalu K, Abera B, Mulu W. Extended spectrum beta lactamase producing bacteria among outpatients with Ear infection at FelegeHiwot Referral Hospital, North West Ethiopia. PLoS One 2020; 15 (9): e0238891.
3. Buhaibeh Q, Dhaiban T, Alyafei E, Al-Jundi Abdulsalam AS. Bacterial profile and antimicrobial susceptibility patterns of otitis media among children in Qatar. Int J Res Med Sci 2019; 7: 3311-3316.
4. Ejiofor SO, Edeh AD, Ezeudu CE, Gugu TH, Oli AN. Multi-drug resistant acute otitis media amongst children attending out-patient clinic in Chukwuemeka Odumegwu Ojukwu University Teaching Hospital, Awka, South-East Nigeria. Adv Microbiol 2016; 6: 495-501.
5. Tesfa T, Mitiku H, Sisay M, Weldegebreal F, Ataro Z, Motbaynor B, et al. Bacterial otitis media in sub-Saharan Africa: A systematic review and meta-analysis. BMC Infect Dis 2020; 20: 225.
6. Akinjogunla OJ, Eghafona NO, Enabulele IO. Aetiologic agents of acute otitis media (AOM): prevalence, antibiotic susceptibility, beta-lactamase (Βl) and extended spectrum beta-lactamase (ESBL) production. J Microbiol Biotechnol Food Sci 2011; 1: 333-353.
7. Khatoon A, Rizvi M, Sultan A, Khan F, Sharma M, Shukla I, et al. Chronic suppurative otitis media: A clinico-microbiological Menace. Int J Res Med Sci 2015; 3: 1932-1936.
8. Teklu DS, Negeri AA, Legese MH, Bedada TL, Woldemariam HK, Tullu KD. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrob Resist Infect Control 2019; 8: 39.
9. Pfeifer Y, Cullik A, Witte W. Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 2010; 300: 371-379.
10. Walsh TR, Toleman MA, Poirel L, Nordmann P. Metallo-β- lactamases: The Quiet before the storm? Clin Microbiol Rev 2005; 18: 306-325.
11. El-Hady SA, Adel LA. Occurrence and detection of AmpC β-lactamases among Enterobacteriaceae isolates from patients at Ain Shams University Hospital. Egypt J Med Hum Genet 2015; 16: 239-244.
12. Chika E, Charles E, Ifeanyichukwu I, Michael A. First Detection of FOX-1 AmpC β-lactamase gene expression among Escherichia coli isolated from abattoir samples in Abakaliki, Nigeria. Oman Med J 2018; 33: 243-249.
13. Nnaji JO, Moses IB, Ejikeugwu PC, Nwakaeze EA, Ude-Ude I, Iroha IR. Antibiogram and molecular characterization of AmpC and ESBL-producing Gram-negative bacteria from poultry and abattoir samples. Pak J Biol Sci 2021; 24: 193-198.
14. Orji JN (2011). Political Organization in Nigeria since the Late Stone Age: A History of the Igbo People, Palgrave Macmillan, 2011th Edition, New York.
15. The World Gazetteer (2013). https://archive.is/20130209150810/http://www.world-gazetteer.com/wg.php. Accessed 10 November, 2022.
16. Molla R, Tiruneh M, Abebe W, Moges F. Bacterial profile and antimicrobial susceptibility patterns in chronic suppurative otitis media at the University of Gondar Comprehensive Specialized Hospital, Northwest Ethiopia. BMC Res Notes 2019; 12: 414.
17. World Medical Association (WMA). Declaration of Helsinki. Ethical principles for medical research involving human subjects. Note of Clarification on paragraph 30 added by the WMA General Assembly, Tokyo; 2004.
18. Cheesbrough M (2006). District Laboratory Practice in Tropical Countries (Part II), Cambridge University.
19. Moses IB, Ugbo EN, Odah EE, Iroha IR, Agumah NB, Ukpai EG, et al. Antibiogram and phenotypic characterization of E. coli isolated from Nigeria’s paper currencies obtained from Butchers in Ebonyi State. Arch Clin Microbiol 2018; 9: 85.
20. Iroha IR, Mohammed ID, Moses IB, Ngwu NJ, Uzoeto HO, Oladimeji AS, et al. Molecular characterization of Enterobacteriaceae isolated from gingivitis and periodontitis patients and the antimicrobial activity of mouth wash agents. Sci Afr 2022; 15: e01106.
21. Clinical Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 27th Edition, CLSI supplements M100Wayne: Clinical and Laboratory Standards Institute; 2017.
22. Moses IB, Esimone CO, Iroha IR, Ugbo EN, Orji JO, Nwuzo AC, et al. First report on the antibiotic resistance profiles and virulence genes of Staphylococcus pseudintermedius colonizing dogs and humans in Abakaliki, South-East Nigeria. Res J Microbiol 2020; 15: 22-34.
23. Moses IB, Esimone CO, Iroha IR, Rubin JE, Sniatynsky MK, Ribeiro ACS, et al. Antibiotypes and high frequency of toxin genes in methicillin-resistant Staphylococcus pseudintermedius from nares of dogs and dog guardians in Nigeria. Comp Immunol Microbiol Infect Dis 2022; 89: 101870.
24. Singh BR, Pradhan S, Murthy R, Agrawal E, Barapatre R, Kumari N, et al. Emergence of antibiotic resistance in bacteria isolated from Tubotympanic type of chronic suppurative otitis media in Chhattisgarh. Int J Otorhinolaryngol Head Neck Surg 2019; 5: 1674-1678.
25. Fayemiwo SA, Ayoade RA, Adesiji YO, Taiwo SS. Pattern of bacterial pathogens of acute otitis media in a tertiary Hospital, South Western Nigeria. African J Clin Exp Microbiol 2017; 18: 29- 34.
26. Nnebe-Agumadu U, Okike O, Orji I, Ibekwe RC. Childhood suppurative otitis media in Abakaliki: isolated microbes and in vitro antibiotic sensitivity pattern. Niger J Clin Pract 2011; 14: 159-162.
27. Prakash R, Juyal D, Negi V, Pal S, Adekhandi S, Sharma M, et al. Microbiology of chronic suppurative otitis media in a tertiary care setup of Uttarakhand State India. N Am J Med Sci 2013; 5: 282-287.
28. Kazeem MJ, Aiyeleso R. Current Bacteriological Profile of chronic suppurative otitis media in a tertiary facility of Northern Nigeria. Indian J Otol 2016; 22: 157-161.
29. Chirwa M, Mulwafu V, Aswani JM, Masinde V, Mkakosya R, Soko D. Microbiology of chronic suppurative otitis media at Queen Elizabeth Central Hospital, Blantyre, Malawi: A cross-sectional descriptive study. Malawi Med J 2015; 27: 120-124.
30. Amiri-Andy SA, Sarokhani D, Azami M, Vazini H, Rezaei-Tavirani M, Dehkordi AH. Systematic review and meta-analysis of otitis media in Iran: prevalence, etiology, antibiotic susceptibility, and complications. Indian J Otol 2018; 24: 1-8.
31. Gupta P, Varshney S, Kumar SK, Mohanty A, Jha MK. Chronic suppurative otitis media: A microbiological review of 20 years. Indian J Otol 2020; 26: 59-67.
32. Mansoor T, Musani MA, Khalid G, Kamal M. Pseudomonas aeruginosa in chronic suppurative otitis media: sensitivity spectrum against various antibiotics in Karachi. J Ayub Med Coll Abbottabad 2009; 21: 120-123.
33. Poorey VK, Iyer A. Study of bacterial Flora in chronic suppurative otitis media and its clinical significance. Indian J Otolaryngol Head Neck Surg 2002; 54: 91-95.
34. Adesoji AT, Ogunjobi AA, Olatoye IO. Molecular characterization of selected multidrug resistant Pseudomonas from water distribution systems in southwestern Nigeria. Ann Clin Microbiol Antimicrob 2015; 14: 39.
35. Onuoha SC. The prevalence of antibiotic resistant diarrhogenic bacterial species in surface waters, South Eastern Nigeria. Ethiop J Health Sci 2017; 27: 319-330.
36. Onifade AK, Afolayan CO, Afolami OI. Antimicrobial sensitivity, extended spectrum beta-lactamase (ESBL) production and plasmid profile by microorganisms from otitis media patients in Owo and Akure, Ondo State, Nigeria. Karbala Int J Mod Sci 2018; 4: 332-340.
37. Manoharan A, Sugumar M, Kumar A, Jose H, Mathai D, Khilnani GC, et al. Phenotypic & molecular characterization of AmpC β-lactamases among Escherichia coli, Klebsiella spp. & Enterobacter spp. from five Indian Medical Centers. Indian J Med Res 2012; 135: 359-364.
38. Helmy MM, Wasfi R. Phenotypic and molecular characterization of plasmid mediated AmpC β-lactamases among Escherichia coli, Klebsiella species, and Proteus mirabilis isolated from urinary tract infections in Egyptian hospitals. Biomed Res Int 2014; 2014: 171548.
| Files | ||
| Issue | Vol 15 No 6 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i6.14139 | |
| Keywords | ||
| AmpC-β-lactamase; Chronic suppurative otitis media; Gram-negative bacterial pathogens; FOX-AmpC gene; Multidrug resistance | ||
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How to Cite
1.
Amadi I, Catherine Nchedo O, Obaji A, Agbonifo M, Eze E, Stacy I, Benjamin M, Romanus I. Detection of FOX-AmpC-β-lactamase gene and antibiogram of AmpC-beta-lactamase-producing pathogens isolated from chronic suppurative otitis media patients in Nigeria. Iran J Microbiol. 2023;15(6):779-787.
